1 INTRODUCTION

Injuries and lesions of the cervical spine are not uncommon.1 The anterior cervical midline (ACM) approach is a commonly utilised technique in patients with underlying degenerative disc disease, cervical radiculopathy, and cervical myelopathy.2 The anterior approach can also be utilised in more complex cases, such as cases of tumour resection and ossification of the posterior longitudinal ligament, or in cases where a posterior approach is not optimal, such as cases of existing kyphosis.3-5

An extremely rare complication of the ACM approach is iatrogenic injury to the esophageal oropharyngeal region. This could be caused by intubation or direct surgical trauma intraoperatively. Yadav2 analysed postoperative complications following anterior cervical discectomy and fusion (ACDF) and found that one patient (1/128, 0.78%) suffered pharyngeal perforation and presented postoperatively with subcutaneous emphysema and haemoptysis.

The anterior cervical retropharyngeal (ACR) approach is indicated in cases involving the anterior cervical spine, including cases of tumour resection, abscess drainage, atlantoaxial subluxation, decompression, and stabilisation. Its main advantage over posterior approaches is easy positioning and minimal need for soft tissue dissection. The ACR approach provides wide exposure (of the anterior upper cervical spine, lower clivus, and brainstem region) and feasibility for instrumentation.6

However, the limited space in which important neurovascular and visceral structures course and overlap contributes to the complexity of the anatomy, resulting in high difficulty, high risk, and various perioperative complications.7 Posterior pharyngeal wall defects (PPWDs) is one of the most frequently encountered surgical morbidities after surgery with the ACR approach and can lead to prolonged inpatient hospital stays, delay in the onset of oral feeding and increase in the overall cost of treatment.8

Various vascularised tissue flaps have been tried. Traditional methods for repair of the posterior pharyngeal wall include the pectoralis major myocutaneous flap, the platysma myocutaneous flap, the submental flap, the facial artery flap, the supraclavicular island flap, and free flaps. Andres9 reported that a PPWD after the excision of a chordoma and postoperative radiotherapy was successfully resolved with a free fibular osteo-adipofascial flap. Li10 found that the application of a posterior pharyngeal flap to repair a defect due to a posterior pharyngeal wall carcinoma located at the level of the cricoid cartilage after resection was an effective reconstruction method. However, as far as we known, no study has ever performed regarding the role of the sternocleidomastoid (SCM) myocutaneous flap in PPWD repair.

The purpose of this report was to retrospectively analyse the treatment efficacy of an island SCM myocutaneous flap (ISMF) in the surgical management of a PPWD after anterior cervical spine surgery (ACSS), which was previously unreported.

2 PATIENTS AND ETHIC STATEMENT

We retrospectively reviewed medical records and imaging studies of three patients who underwent PPWD repair after ACSS with the ISMF at the Peking University Third Hospital from November 2016 to November 2019. The study was approved by the Ethics Committee of Peking University Third Hospital (No. IRB00006761-M2020576).

A brief overview of the relevant technical surgical data is provided, followed by a description of the management of these three cases. All cases signed informed consents for publication.

3 CASE REPORT 3.1 Surgical procedure

Tracheotomy and debridement assisted by a mouth opener were the first and key steps in the operation. Surgical reoperation was performed through the previous oblique incision along the anterior border of the SCM. This incision was carried deep through the platysmal muscle, and subplatysmal flaps were raised superiorly and inferiorly. The SCM was then identified and freed from the investing deep cervical fascia through an anterior border incision. The spinal accessory nerve was identified and preserved, with standard care for the preservation of the recurrent laryngeal nerve. Depending on the location and size of the lesion, the SCM might be harvested with an inferiorly or superiorly based pedicled flap (inferior pedicled flaps for the lower cervical spine; superior pedicled flaps for the upper cervical spine).11, 12 Once the flap was sufficiently mobilised, it was rotated into the defect. The muscle was sutured onto the longus colli fascia and available prevertebral fascia. After assuring haemostasis and confirming obliteration of the dead space, a drain was placed, and the platysmal muscle was closed. Layered wound closure was then performed.

During the operation, placing the ISMF into the defect of the posterior pharyngeal wall was the most difficult process. The author applied the method of the intraextra-oral combination to insert the flap into the PPWD. Obtuse separation was performed outside the mouth, along the inside of the cervical sheath, next to the tracheal side, until reaching the prevertebral fascia of the cervical vertebra. The prevertebral fascia was cut open, and then obtuse dissection was performed at the deep side to the defect site. In the mouth, blunt dissection of the prevertebral fascia was performed approximately 2–3 cm below the defect. Then, the flap was inserted 2–3 cm below the defect of the posterior pharyngeal wall into the mouth. It was necessary to avoid damage to the vagus nerve during the process. Dr Yang, whose working experience of over 20 years, performed the surgery. The flow chart of the surgical procedure is shown in Figure 1.

The flow chart of surgical procedure. A, PPWD could be seen through the mouth (the arrow points to PPWD). B, The upper ISMF was designed, with an area of 10 × 4 cm2. The dotted line was the area where the epidermis was removed. C, The sternal head and clavicle head were cut off, and the vessel pedicle was rotated about 2 cm below the mastoid process. D, Blunt dissection of the prevertebral fascia was performed, and the flap was inserted into the mouth through the prevertebral space (the arrow points to ISMF). E, The ISMF was placed in the mouth and sutured (the arrow points to ISMF). F, The incision was sutured and subfascial drainage was placed. G, Mucosalisation began to occur on the surface of the skin 4 months after operation (the arrow points to ISMF). H, The ISMF survived well, the donor scar was acceptable, and the neck shape and function were unaffected 12 months after operation. ISMF, island sternocleidomastoid myocutaneous flap; PPWD, posterior pharyngeal wall defect

3.2 Observational indexes

The observational indexes are as follows: postoperative survival of the flap, wound healing 2 weeks after surgery, eating, and pronunciation function 2 months after surgery.

3.3 Case 1

A 48-year-old female with atlantoaxial joint dislocation, high cervical myelopathy, and odontoid fracture due to trauma was evaluated in November 2014. She subsequently underwent atlantoaxial joint release with the ACR approach and posterior atlantoaxial lateral mass screw fixation on December 1, 2014. Due to poor postoperative neurological recovery, the patient underwent revision surgery on December 3, 2014, March 17, 2015, and April 2, 2015. In the last revision operation, cerebrospinal fluid (CSF) leakage was caused by separation of the axis from the free odontoid process. During the operation, a lumbar subarachnoid drain was placed, and haemostatic gauze was used for durotomy coverage. The patient presented classic findings, including fever, persistent leukocytosis, elevated C-reactive protein, and abnormal sensation in the mouth, and the drainage volume of the lumbar cistern was too small after the first several days postoperatively. Computed tomography (CT) demonstrated a large area of CSF reaccumulation in her anterior neck.

The patient returned to the operating room for instrumentation removal and further exploration. After intraoperative exposure of the posterior pharyngeal wall, the incision from the previous operation was split, and the anterior atlantoaxial arch and axial body were exposed. There was fluid accumulation in the space between the atlantoaxial vertebrae, and the soft tissue tension on both sides was high, which made direct suturing impossible. Therefore, the upper ISMF was designed, with an area of 10 × 4 cm2. The sternal head and the clavicular head were cut off, and the ISMF was rotated approximately 2 cm below the mastoid process to enter the oral cavity from the medial side of the mandible. Meanwhile, muscle tissue and several portions of fascial tissue from the free part of the ISMF were used to fill the bone space between the atlantoaxial vertebrae to block the durotomy. The flap was properly trimmed and sutured with the incision in the posterior pharyngeal wall. Both sides of the flap donor site were free and sutured directly. Layered closure was then performed. One subfascial drain was used.

The patient's postoperative outcomes were as follows. The drain was removed on postoperative day 3, and the stitches were taken out 14 days after the operation. The patient's eating and pronunciation functions were recovered well after the removal of the nasogastric tube 2 months after the operation. Four months after the operation, mucosalisation began to occur on the surface of the skin. Twelve months after the operation, cervical spine MRI showed the ISMF survived well, the donor site scar was acceptable, and the neck shape and function were unaffected. The cervical spine MRI imaging 5 years after surgery showed that ISMF was seen on the posterior pharynx wall, the flap was stable, and the PPWD healed well (Figure 2).

The MRI imaging of case 1. A, Sagittal view of cervical spine (12 months after surgery): ISMF (arrow) was seen on the posterior pharynx wall and the flap survived well. B, Sagittal view of cervical spine (5 years after surgery): ISMF (arrow) was seen on the posterior pharynx wall, the flap was stable, and the PPWD healed well. ISMF, island sternocleidomastoid myocutaneous flap; PPWD, posterior pharyngeal wall defect

3.4 Case 2

Due to a C2 paravertebral chordoma, a 57-year-old male underwent staged posterior C2 laminectomy and attachment resection, C1-3 lateral mass screw fixation, anterior C2 vertebral body and prevertebral tumour resection, and C1-3 intervertebral artificial vertebral body implantation and pedicle screw fixation. The posterior pharyngeal wall was torn during tracheal extubation after surgery with the anterior approach. Therefore, repair was subsequently performed. Four days after the operation, the patient experienced recurrence of a local tear in the repaired posterior pharyngeal wall, and conservative treatment was ineffective.

The patient underwent surgical repair with an ISMF after 2 weeks of non-healing of the PPWD. During the operation, the area of the PPWD was found to be approximately 6 × 4 cm2, and the three dimensions (3D)-printed prosthesis was exposed. After thorough debridement, the ISMF was designed with a size of 11 × 4 cm2.

The trachea was extubated 3 weeks after surgery, and oral feeding was resumed 2 months after surgery. The CT scan of the cervical spine at 1 month after the operation and the MRI imaging at 4 months after the operation showed that the ISMF survived and the PPWD healed well. The imaging figures before and after the operation are shown in Figure 3. No obvious pharyngeal foreign body sensation was observed, and the wound showed satisfactory healing at the follow-up 1 year after the operation.

Imaging data of case 2. A, MRI sagittal view of the cervical spine; B, CT sagittal view; and C, CT transverse view: There was a marked defect (arrow) in the posterior pharyngeal wall before surgery. D, CT sagittal view; E, CT transverse view: The flap (arrow) survived well and the defect was repaired 1 month after IMSF repairment surgery. F, MRI sagittal view; G, MRI transverse view: The flap (arrow) survived well and the defect was repaired 4 months after surgery. CT, computerised tomography; IMSF, island sternocleidomastoid myocutaneous flap; MRI, magnetic resonance imaging

3.5 Case 3

A 49-year-old man presented with cervical and shoulder pain, and a C2-6 chordoma, secondary spinal stenosis, and pathological fracture of the C4 vertebral body were found. In September 2019, he underwent posterior C2-7 laminectomy and attachment resection with pedicle screw fixation from the occiput to T3. In October 2019, he underwent discectomy at C2-3, C2 odontoid base osteotomy, and partial odontoid resection, en bloc sacrectomy of C2 by the ACR approach, discectomy at C7-T1 combined with the anterior cervical submandibular approach, C3-7 vertebral body free and total resection, and 3D-printed prosthesis implantation. Ten days after the operation, the patient presented obvious foreign body sensation in the pharynx, along with increased oropharyngeal secretion. Physical examination revealed dehiscence of the oropharyngeal incision, and he subsequently underwent reconstruction with the ISMF after tracheotomy. The flap was designed with an area of 11.5 × 3.5 cm2 according to the PPWD size of 5 × 2 cm2. The CT scan of the cervical spine at 1 month after the operation and the MRI imaging at 4 months after the operation showed that the ISMF survived and the PPWD healed well. The imaging figures before and after the operation are shown in Figure 4. At his 1-year postoperative visit, he was in good condition, with no residual sequelae.

Imaging data of case 3. A, CT sagittal view of the cervical spine; B, CT transverse view: There was a defect (arrow) in the posterior pharyngeal wall, and the prosthesis was exposed. C, CT sagittal view; D, CT transverse view: PPWD was repaired, and the flap (arrow) survived well 1 month after surgery. E, MRI sagittal view: The flap survived well 4 months after surgery. CT, computerised tomography; MRI, magnetic resonance imaging; PPWD, posterior pharyngeal wall defect

3.6 Follow-up outcomes

These three patients tolerated the aforementioned procedure and did not require any further procedures related to the PPWD. The patients experienced no long-term sequelae and were doing well at the 1-year follow-up. None of the patients experienced functional limitations related to the use of the ISMF. The clinical characteristics of these cases are shown in Table 1.

TABLE 1. The clinical characteristics of three cases Case 1 Case 2 Case 3 Age 48 57 49 Gender Female Male Male Initial surgical approach ACR Posterior ACR ISMF size (cm2) 10 × 4 11 × 4 11.5 × 3.5 Follow-up duration 5 years 1 year 1 year Flap condition ISMF survived well ISMF survived well ISMF survived well PPWD healing PPWD healed well PPWD healed well PPWD healed well Abbreviations: ACR, anterior cervical retropharyngeal; ISMF, island sternocleidomastoid myocutaneous flap; PPWD, posterior pharyngeal wall defects. 4 DISCUSSION

Two of the three patients underwent surgery with the ACR approach, and one patient underwent surgery with the ACM approach. The posterior pharyngeal wall was torn during tracheal extubation in the patient who underwent surgery with the ACM approach. All three patients suffered from a PPWD, one of whom had a PPWD with CSF leakage, and the other two patients had a PPWD with 3D-printed prosthesis exposure.

CSF leakage and dural tears following surgery with the ACM or ACR approach are rare complications that occur in 0.2% to 1% of patients postoperatively.13 Hannallah et al14 focused on cervical spine dural tears, noting a 1% incidence among 2216 procedures. Although the overall incidence of durotomy is generally lower in cervical spine procedures, primary repair is often much more difficult given the limited exposure.15 Our study revealed that the ISMF is useful as a reinforcement in the repair of persistent cervical durotomy after surgery with the ACR approach. In case 1, the patient had no evidence of persistent CSF leakage after repairment surgery. The muscle flap was used to augment our repair and to decrease the postsurgical dead space. Although we do not recommend this procedure in primary durotomy repair in the anterior cervical spine, the ISMF might be useful to augment repair in cases of persistent CSF leakage refractory to conventional management.

The medical implications of 3D printing technology have evolved, and this technology has been increasingly used. At times, surgical spine oncology involves complex resection using various surgical approaches and unique spinal reconstruction. 3D printing technology allows improvements in preoperative planning, the practice and exploration of various surgical approaches and the design of customised surgical tools and patient-specific implants.16, 17 However, the implantation of a prosthesis is generally associated with an inflammatory foreign body reaction.18 If prolonged inflammation develops after implantation, it might lead to clinical complications, such as defective wound healing, damage to the implant, and the need for reoperation.19 Perhaps a PPWD and exposure are critical for 3D-printed prostheses, and prosthesis coverage by various vascularised tissue flaps is necessary. We presented the first report of the ISMF in PPWD repair after cervical spine surgery and found that the flap was significantly useful in repair of the PPWD and exposure of the 3D-printed prothesis.

The SCM originates from the sternum and clavicle, runs obliquely upward, and ends at the mastoid process and superior nuchal line of the temporal bone.20 The initial part of the sternal head is mostly tendinous, approximately 3.3 cm long and 1.2 cm wide, starting from the upper quarter of the ipsilateral front of the manubrium sternum, and generally muscular at the upper margin of the medial end of the manubrium sternum and clavicle. The clavicular head starts from the medial 1/3 of the medial half of the clavicle. The medial end of the initial position is 1.1 cm away from the medial end of the clavicle, and the lateral end of the starting point is 2.5 cm away from the midpoint of the clavicle. The clavicular head is myogenic, which is conducive to the formation of an osteogenic-myocutaneous flap. The clavicle in the flap is mainly the medial half of the clavicle, and the medial end of the clavicle should be retained in situ to preserve the function of the sternoclavicular joint.21

The blood supply of SCM is segmental. The arterial supply has three sources: upper, middle, and lower, that is, the occipital artery (OCA), the superior thyroid artery (STA), and the branch of the thyroid trunk (the branch of the transverse carotid artery), respectively.22 The external jugular vein passes inferiorly and posteriorly through the SCM, from which it drains venous blood (external posterior jugular vein and anterior jugular vein).23 The blood supply characteristics of the SCM enable the flap to have two rotation axes, namely, the upper pedicled flap based on the OCA and the lower pedicled flap based on the transverse carotid artery. The blood supply of ISMF is shown in Figure 5.

The blood supply of ISMF. Schematic drawing of all arteries supplying the sternocleidomastoid (SCM) muscle. ACA, ascending cervical artery; ECA, external carotid artery; ISMF, island sternocleidomastoid myocutaneous flap; ITA, inferior thyroid artery; OCA, occipital artery; SA, suprascapular artery; SAN, spinal accessory nerve; STA, superior thyroid artery; TT, thyrocervical trunk. Modified and with permission from Kierner et al24

The ISMF can be used as a myocutaneous, myofascial, myoperiosteal, or osteomuscular flap.25 The first SCM flap operation was reported in 1908. Surgical outcomes have been variable, largely a result of the variable blood supply to the muscle.26 The main advantages are that it requires a shorter operative duration than free flaps,27 has reduced muscle bulk, is associated with reduced morbidity, and is a convenient, versatile, and hairless tissue.28 Currently, the ISMF is used in many situations when it is necessary to repair or reconstruct the orofacial and pharyngeal areas. Some muscular flaps or flaps with bony portions are used, depending on the surgical objective. Examples of reconstructive interventions are as follows: (a) reconstruction of the tongue and/or buccal floor; (b) reconstruction of the oral cavity, oropharynx, and/or laryngotracheal complex; (c) reconstruction of portions of the head and/or neck; (d) reconstruction of bone of the jaw or defects in the mastoid area; (e) reconstruction of the esophagopharyngeal complex; and (f) reconstruction of the cheek.25 Another surgical context in which the ISMF is used is in the presence of congenital muscular torticollis, although the cause is not entirely understood.29 The controversy regarding the use of the SCM flap has centred on the high rate of ischemic complications.30 Complication rates vary considerably, although they have apparently decreased in recent years. As it is difficult to compare studies, because of the differing techniques, flap types, and defects described, the techniques that decrease complications are hard to elucidate. In our study, the three patients did not have any postoperative complications, including flap necrosis, wound non-union, and other complications after repair with the ISMF, and did not require any further surgical procedures related to the cervical spine.

We designed a flap with a size range of approximately 10 × 4 cm2 to repair the PPWD after ACSS. The length of the flap floated 1–2 cm according to the longitudinal diameter of the defect, and a width of 4 cm could ensure the repair of the transverse defect. Meanwhile, the donor area could be directly sutured without the need for skin grafting. During dissection, the spinal accessory nerve innervation and the upper OCA blood supply to the flap were preserved. The ISMF was rotated approximately 2 cm below the mastoid to ensure that at least the flap from the OCA blood supply was reliable. The blood supply to the middle third of the SCM via the STA and external carotid artery branches was expected to be partially or completely ligated, and vascular pedicles of the suprascapular artery to the lower portion of the SCM were unavoidably sacrificed.24

There are obvious advantages of the ISMF in PPWD repair, as follows: (a) the ISMF has a rich and reliable blood supply to ensure a high survival rate, therefore its role in PPWD repair is reliable; (b) the area of the PPWD is relatively small, generally less than 5 × 4 cm2, so the ISMF can be designed as a single-pedicle island flap with a long muscle pedicle and flexible rotation; (c) the thickness of the ISMF is moderate, which is beneficial to the recovery of swallowing function; and (d) the ISMF causes relatively little trauma and rapid recovery and does not even affect the synchronous cervical lymph node dissection.

4.1 Limitations

Although our experience showed ISMF is a feasible and safety technique in repairing PPWDs, the limited number of cases is an unavoidable problem. Furthermore, relatively short follow-up period and retrospective nature is also a limitation.

5 CONCLUSION

The findings described in this work represented the satisfactory outcomes of a new method for PPWD repair after ACSS. It may provide a new option for the treatment of complications after ACSS.

CONFLICT OF INTEREST

The authors declared no potential conflicts of interest.

AUTHOR CONTRIBUTIONS

XLZ and XY contributed to the conception and design of the study; RLZ and YJ C performed the experiments, PBD and YZ collected and analysed data; XLZ and XY wrote the manuscript. All authors reviewed and approved the final version of the manuscript.